Home LiteratureArticle Details
PMID: 8195287 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Involvement of 70-kD heat-shock proteins in peroxisomal import.

The Journal of cell biology ·Vol. 125 ·No. 5 ·1994-06-00 ·Pages 1037-46

Walton PA, Wendland M, Subramani S, Rachubinski RA, Welch WJ

Abstract

This report describes the involvement of 70-kD heat-shock proteins (hsp70) in the import of proteins into mammalian peroxisomes. Employing a microinjection-based assay (Walton, P. A., S. J. Gould, J. R. Feramisco, and S. Subramani. 1992. Mol. Cell Biol. 12:531-541), we demonstrate that proteins of the hsp70 family were associated with proteins being imported into the peroxisomal matrix. Import of peroxisomal proteins could be inhibited by coinjection of antibodies directed against the constitutive hsp70 proteins (hsp73). In a permeabilized-cell assay (Wendland and Subramani. 1993. J. Cell Biol. 120:675-685), antibodies directed against hsp70 proteins were shown to inhibit peroxisomal protein import. Inhibition could be overcome by the addition of exogenous hsp70 proteins. Purified rat liver peroxisomes were shown to have associated hsp70 proteins. The amount of associated hsp70 was increased under conditions of peroxisomal proliferation. Furthermore, proteinase protection assays indicated that the hsp70 molecules were located on the outside of the peroxisomal membrane. Finally, the process of heat-shocking cells resulted in a considerable delay in the import of peroxisomal proteins. Taken together, these results indicate that heat-shock proteins of the cytoplasmic hsp70 family are involved in the import of peroxisomal proteins.

MeSH Terms
Animals Biological Transport Blotting, Western Cell Line Endopeptidase K Fluorescent Antibody Technique Heat-Shock Proteins/chemistry,metabolism Hot Temperature Humans Liver/metabolism Microbodies/metabolism Rats Serine Endopeptidases/pharmacology
Chemicals
Heat-Shock Proteins Serine Endopeptidases Endopeptidase K
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Walton P A
Department of Anatomy and Cell Biology, McGill University, Montreal, Canada.
Wendland M
Subramani S
Rachubinski R A
Welch W J
References (60)
60 references, click to expand
  1. The two mammalian mitochondrial stress proteins, grp 75 and hsp 58, transiently interact with newly synthesized mitochondrial proteins.
    Cell Regul. 1991 Feb;2(2):165-79 PMID: 1677814
  2. SSC1, an essential member of the yeast HSP70 multigene family, encodes a mitochondrial protein.
    Mol Cell Biol. 1989 Jul;9(7):3000-8 PMID: 2674677
  3. Characterization of the integral membrane polypeptides of rat liver peroxisomes isolated from untreated and clofibrate-treated rats.
    Biochem Cell Biol. 1991 Aug;69(8):499-508 PMID: 1760154
  4. Transport of microinjected proteins into peroxisomes of mammalian cells: inability of Zellweger cell lines to import proteins with the SKL tripeptide peroxisomal targeting signal.
    Mol Cell Biol. 1992 Feb;12(2):531-41 PMID: 1732729
  5. Antifolding activity of hsp60 couples protein import into the mitochondrial matrix with export to the intermembrane space.
    Cell. 1992 Mar 20;68(6):1163-75 PMID: 1347713
  6. The transport of proteins into the nucleus requires the 70-kilodalton heat shock protein or its cytosolic cognate.
    Mol Cell Biol. 1992 May;12(5):2186-92 PMID: 1569948
  7. The role of heat-shock proteins as molecular chaperones.
    Curr Opin Cell Biol. 1991 Dec;3(6):1033-8 PMID: 1687649
  8. Synthesis of catalase in two cell-free protein-synthesizing systems and in rat liver.
    Proc Natl Acad Sci U S A. 1978 Sep;75(9):4344-8 PMID: 279920
  9. Biogenesis of peroxisomes: intracellular site of synthesis of catalase and uricase.
    Proc Natl Acad Sci U S A. 1978 Oct;75(10):5066-70 PMID: 368807
  10. In vivo phosphorus-31 nuclear magnetic resonance reveals lowered ATP during heat shock of Tetrahymena.
    Science. 1983 Mar 11;219(4589):1223-5 PMID: 6828852
  11. Biochemical characterization of the mammalian stress proteins and identification of two stress proteins as glucose- and Ca2+-ionophore-regulated proteins.
    J Biol Chem. 1983 Jun 10;258(11):7102-11 PMID: 6406494
  12. Nuclear and nucleolar localization of the 72,000-dalton heat shock protein in heat-shocked mammalian cells.
    J Biol Chem. 1984 Apr 10;259(7):4501-13 PMID: 6368558
  13. Biosynthesis and intracellular transport of enzymes of peroxisomal beta-oxidation.
    J Biol Chem. 1984 May 25;259(10):6397-402 PMID: 6725256
  14. Alcohol oxidase assembles post-translationally into the peroxisome of Candida boidinii.
    J Biol Chem. 1984 Jul 10;259(13):8485-93 PMID: 6376510
  15. Biosynthesis and regulation of the peroxisomal methanol oxidase from the methylotrophic yeast Hansenula polymorpha.
    Mol Gen Genet. 1984;194(3):489-93 PMID: 6377014
  16. Acyl-Coa oxidase and hydratase-dehydrogenase, two enzymes of the peroxisomal beta-oxidation system, are synthesized on free polysomes of clofibrate-treated rat liver.
    J Cell Biol. 1984 Dec;99(6):2241-6 PMID: 6501422
  17. Protein folding in mitochondria requires complex formation with hsp60 and ATP hydrolysis.
    Nature. 1989 Sep 14;341(6238):125-30 PMID: 2528694
  18. A role for a 70-kilodalton heat shock protein in lysosomal degradation of intracellular proteins.
    Science. 1989 Oct 20;246(4928):382-5 PMID: 2799391
  19. Polypeptide chain binding proteins: catalysts of protein folding and related processes in cells.
    Cell. 1989 Nov 17;59(4):591-601 PMID: 2573430
  20. Peroxisomal protein import is conserved between yeast, plants, insects and mammals.
    EMBO J. 1990 Jan;9(1):85-90 PMID: 2104803
  21. The 70-kDa peroxisomal membrane protein is a member of the Mdr (P-glycoprotein)-related ATP-binding protein superfamily.
    J Biol Chem. 1990 Mar 15;265(8):4534-40 PMID: 1968461
  22. Interaction of Hsp 70 with newly synthesized proteins: implications for protein folding and assembly.
    Science. 1990 May 18;248(4957):850-4 PMID: 2188360
  23. Mitochondrial precursor protein. Effects of 70-kilodalton heat shock protein on polypeptide folding, aggregation, and import competence.
    J Biol Chem. 1990 Jul 5;265(19):11069-76 PMID: 2193031
  24. Latency of the peroxisomal enzyme acyl-CoA:dihydroxyacetonephosphate acyltransferase in digitonin-permeabilized fibroblasts: the effect of ATP and ATPase inhibitors.
    Biochem Biophys Res Commun. 1990 Aug 16;170(3):1135-43 PMID: 2143898
  25. How do polypeptides cross the mitochondrial membranes?
    Cell. 1990 Nov 2;63(3):447-50 PMID: 2225059
  26. Requirement for hsp70 in the mitochondrial matrix for translocation and folding of precursor proteins.
    Nature. 1990 Nov 8;348(6297):137-43 PMID: 2234077
  27. Molecular cloning and deduced amino acid sequence of nonspecific lipid transfer protein (sterol carrier protein 2) of rat liver: a higher molecular mass (60 kDa) protein contains the primary sequence of nonspecific lipid transfer protein as its C-terminal part.
    Proc Natl Acad Sci U S A. 1991 May 15;88(10):4338-42 PMID: 2034675
  28. Interaction of hsp70 with unfolded proteins: effects of temperature and nucleotides on the kinetics of binding.
    Proc Natl Acad Sci U S A. 1991 Jul 1;88(13):5719-23 PMID: 1829527
  29. Examining the function and regulation of hsp 70 in cells subjected to metabolic stress.
    J Cell Biol. 1992 Jun;117(6):1137-50 PMID: 1607378
  30. Transport of microinjected alcohol oxidase from Pichia pastoris into vesicles in mammalian cells: involvement of the peroxisomal targeting signal.
    J Cell Biol. 1992 Aug;118(3):499-508 PMID: 1639840
  31. The translation machinery and 70 kd heat shock protein cooperate in protein synthesis.
    Cell. 1992 Oct 2;71(1):97-105 PMID: 1394434
  32. Chaperonin-mediated protein folding: GroES binds to one end of the GroEL cylinder, which accommodates the protein substrate within its central cavity.
    EMBO J. 1992 Dec;11(13):4757-65 PMID: 1361169
  33. Function in protein folding of TRiC, a cytosolic ring complex containing TCP-1 and structurally related subunits.
    EMBO J. 1992 Dec;11(13):4767-78 PMID: 1361170
  34. Reconstitution of protein translocation from solubilized yeast membranes reveals topologically distinct roles for BiP and cytosolic Hsc70.
    J Cell Biol. 1993 Jan;120(1):95-102 PMID: 8416998
  35. Cytosol-dependent peroxisomal protein import in a permeabilized cell system.
    J Cell Biol. 1993 Feb;120(3):675-85 PMID: 8425896
  36. The constitutive and stress inducible forms of hsp 70 exhibit functional similarities and interact with one another in an ATP-dependent fashion.
    J Cell Biol. 1993 Mar;120(5):1101-12 PMID: 8436586
  37. Putative X-linked adrenoleukodystrophy gene shares unexpected homology with ABC transporters.
    Nature. 1993 Feb 25;361(6414):726-30 PMID: 8441467
  38. Import of firefly luciferase into mammalian peroxisomes in vivo requires nucleoside triphosphates.
    Exp Cell Res. 1993 Mar;205(1):66-75 PMID: 8453999
  39. Synthesis of a major integral membrane polypeptide of rat liver peroxisomes on free polysomes.
    Proc Natl Acad Sci U S A. 1984 Nov;81(22):7127-31 PMID: 6594687
  40. Synthesis of 3-ketoacyl-CoA thiolase of rat liver peroxisomes on free polyribosomes as a larger precursor. Induction of thiolase mRNA activity by clofibrate.
    Biochem J. 1985 Mar 15;226(3):697-704 PMID: 3985942
  41. Post-translational import of fatty acyl-CoA oxidase and catalase into peroxisomes of rat liver in vitro.
    J Biol Chem. 1985 May 10;260(9):5603-9 PMID: 4039322
  42. Rapid purification of mammalian 70,000-dalton stress proteins: affinity of the proteins for nucleotides.
    Mol Cell Biol. 1985 Jun;5(6):1229-37 PMID: 4033650
  43. Cellular and biochemical events in mammalian cells during and after recovery from physiological stress.
    J Cell Biol. 1986 Nov;103(5):2035-52 PMID: 3536957
  44. Proton ionophores prevent assembly of a peroxisomal protein.
    Cell. 1987 Jan 16;48(1):165-73 PMID: 3539364
  45. A proton-translocating adenosine triphosphatase is associated with the peroxisomal membrane of yeasts.
    Arch Microbiol. 1987 Feb;147(1):42-7 PMID: 2883951
  46. Proteins as molecular chaperones.
    Nature. 1987 Jul 30-Aug 5;328(6129):378-9 PMID: 3112578
  47. Translocation of acyl-CoA oxidase into peroxisomes requires ATP hydrolysis but not a membrane potential.
    J Cell Biol. 1987 Dec;105(6 Pt 2):2915-22 PMID: 3693402
  48. A subfamily of stress proteins facilitates translocation of secretory and mitochondrial precursor polypeptides.
    Nature. 1988 Apr 28;332(6167):800-5 PMID: 3282178
  49. 70K heat shock related proteins stimulate protein translocation into microsomes.
    Nature. 1988 Apr 28;332(6167):805-10 PMID: 3282179
  50. Homologous plant and bacterial proteins chaperone oligomeric protein assembly.
    Nature. 1988 May 26;333(6171):330-4 PMID: 2897629
  51. Heat shock is lethal to fibroblasts microinjected with antibodies against hsp70.
    Science. 1988 Oct 21;242(4877):433-6 PMID: 3175665
  52. Detection of an ATPase activity in rat liver peroxisomes.
    Biochem Biophys Res Commun. 1988 Nov 15;156(3):1353-9 PMID: 2973319
  53. Biogenesis of mitochondria.
    Annu Rev Cell Biol. 1988;4:289-333 PMID: 2461720
  54. 70-kD heat shock-related protein is one of at least two distinct cytosolic factors stimulating protein import into mitochondria.
    J Cell Biol. 1988 Dec;107(6 Pt 1):2051-7 PMID: 3058716
  55. Mitochondrial protein import.
    Biochim Biophys Acta. 1989 Jan 18;988(1):1-45 PMID: 2642391
  56. Mitochondrial heat-shock protein hsp60 is essential for assembly of proteins imported into yeast mitochondria.
    Nature. 1989 Feb 16;337(6208):620-5 PMID: 2645524
  57. Peroxisome targeting signal of rat liver acyl-coenzyme A oxidase resides at the carboxy terminus.
    Mol Cell Biol. 1989 Jan;9(1):83-91 PMID: 2927399
  58. A conserved tripeptide sorts proteins to peroxisomes.
    J Cell Biol. 1989 May;108(5):1657-64 PMID: 2654139
  59. Purification of a novel class of coated vesicles mediating biosynthetic protein transport through the Golgi stack.
    Cell. 1989 Jul 28;58(2):329-36 PMID: 2752426
  60. A novel, cleavable peroxisomal targeting signal at the amino-terminus of the rat 3-ketoacyl-CoA thiolase.
    EMBO J. 1991 Nov;10(11):3255-62 PMID: 1680677
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1994-06-00
Pages
1037-46
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2120043
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]